A p53 defect sensitizes various stages of B cell development to lymphomagenesis in mice carrying an IgH 3′ regulatory region-driven c-myc transgene

Journal of Immunology

Volumn 187, Issue 11, 2011, Pages 5772-5782

  Fiancette, Rémi ^a,c   Rouaud, Pauline ^a   Vincent Fabert, Christelle ^a,d   Laffleur, Brice ^a   Magnone, Virginie ^b   Cogné, Michel ^a   Denizot, Yves ^a  

^a CNRS   (France)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; CASPASE 3; CD19 ANTIGEN; CD45 ANTIGEN; CD5 ANTIGEN; CYCLIN D1; CYCLIN D2; CYCLIN D3; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; IMMUNOGLOBULIN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN H; IMMUNOGLOBULIN M; KI 67 ANTIGEN; LEUKOSIALIN; MYC PROTEIN; PROTEIN MSH2; PROTEIN MSH6; PROTEIN P53; SYNDECAN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOC2 GENE; ARPC4 GENE; ARTICLE; B LYMPHOCYTE; BID GENE; BURKITT LYMPHOMA; CANCER SURVIVAL; CARCINOGENESIS; CDK1 GENE; CELL MATURATION; CLONAL VARIATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE CONTROL; GENE EXPRESSION PROFILING; GENE LOCUS; GENE OVEREXPRESSION; GENE SEQUENCE; GENE TRANSLOCATION; GENETIC RECOMBINATION; IMMUNOGLOBULIN GENE; IMMUNOGLOBULIN VARIABLE REGION; IRAK1BP1 GENE; ITSN1 GENE; LEUKOCYTE COUNT; LEUKOCYTOSIS; LST1 GENE; LYAR GENE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; LYMPHOMA; LYMPHOMAGENESIS; MAGED1 GENE; MANTLE CELL LYMPHOMA; MAPKAP1 GENE; MOUSE; MZF1 GENE; NONHUMAN; NOS2 GENE; ONCOGENE C MYC; PAR2G4 GENE; PENETRANCE; PLASMA CELL LYMPHOMA; PRIORITY JOURNAL; PRKCB GENE; PROTEIN DEFECT; PRSS12 GENE; PTGS1 GENE; SLPI GENE; TADA GENE; TGFBETA1 GENE; TRANSGENE; UCHL3 GENE; VDJ RECOMBINATION;

ANIMALS; B-LYMPHOCYTES; CELL SEPARATION; CELL TRANSFORMATION, NEOPLASTIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENES, MYC; IMMUNOGLOBULIN HEAVY CHAINS; LYMPHOMA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REGULATORY SEQUENCES, NUCLEIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSGENES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 82755189259     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102059     Document Type: Article

References (39)

1. Jares, P., D. Colomer, and E. Campo. 2007. Genetic and molecular pathogenesis of mantle cell lymphoma: perspectives for new targeted therapeutics. Nat. Rev. Cancer 7: 750-762. (Pubitemid 47463673)
2. Blum, K. A., G. Lozanski, and J. C. Byrd. 2004. Adult Burkitt leukemia and lymphoma. Blood 104: 3009-3020. (Pubitemid 39507113)
3. Bergsagel, P. L., and W. M. Kuehl. 2001. Chromosome translocations in multiple myeloma. Oncogene 20: 5611-5622.
4. Pinaud, E., M. Marquet, R. Fiancette, S. Péron, C. Vincent-Fabert, Y. Denizot, and M. Cogné. 2011. The IgH locus 3′ regulatory region: pulling the strings from behind. Adv. Immunol. 110: 27-70.
5. Vincent-Fabert, C., R. Fiancette, M. Cogné, E. Pinaud, and Y. Denizot. 2010. The IgH 3′ regulatory region and its implication in lymphomagenesis. Eur. J. Immunol. 40: 3306-3311.
6. Adams, J. M., A. W. Harris, C. A. Pinkert, L. M. Corcoran, W. S. Alexander, S. Cory, R. D. Palmiter, and R. L. Brinster. 1985. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538. (Pubitemid 16173038)
7. Vincent-Fabert, C., R. Fiancette, E. Pinaud, V. Truffinet, N. Cogné, M. Cogné, and Y. Denizot. 2010. Genomic deletion of the whole IgH 3′ regulatory region (hs3a, hs1,2, hs3b, and hs4) dramatically affects class switch recombination and Ig secretion to all isotypes. Blood 116: 1895-1898.
8. Gostissa, M., C. T. Yan, J. M. Bianco, M. Cogné, E. Pinaud, and F. W. Alt. 2009. Long-range oncogenic activation of Igh-c-myc translocations by the Igh 3′ regulatory region. Nature 462: 803-807.
9. Truffinet, V., E. Pinaud, N. Cogné, B. Petit, L. Guglielmi, M. Cogné, and Y. Denizot. 2007. The 3′ IgH locus control region is sufficient to deregulate a c-myc transgene and promote mature B cell malignancies with a predominant Burkitt-like phenotype. J. Immunol. 179: 6033-6042.
10. Vincent, C., V. Truffinet, R. Fiancette, B. Petit, N. Cogné, M. Cogné, and Y. Denizot. 2009. Uncoupling between Ig somatic hypermutation and oncogene mutation in mouse lymphoma. Biochim. Biophys. Acta 1793: 418-426.
11. Yu, J., and L. Zhang. 2005. The transcriptional targets of p53 in apoptosis control. Biochem. Biophys. Res. Commun. 331: 851-858. (Pubitemid 40615516)
12. Martins, C. P., L. Brown-Swigart, and G. I. Evan. 2006. Modeling the therapeutic efficacy of p53 restoration in tumors. Cell 127: 1323-1334. (Pubitemid 44960417)
13. Lowe, S. W., E. M. Schmitt, S. W. Smith, B. A. Osborne, and T. Jacks. 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362: 847-849. (Pubitemid 23132161)
14. Treasure, J., A. Lane, D. B. Jones, and D. H. Wright. 1992. CD43 expression in B cell lymphoma. J. Clin. Pathol. 45: 1018-1022.
15. Vincent-Fabert, C., V. Truffinet, R. Fiancette, N. Cogné, M. Cogné, and Y. Denizot. 2009. Ig synthesis and class switching do not require the presence of the hs4 enhancer in the 39 IgH regulatory region. J. Immunol. 182: 6926-6932.
16. Le Brigand, K., and P. Barbry. 2007. Mediante: a web-based microarray data manager. Bioinformatics 23: 1304-1306. (Pubitemid 47050552)
17. Le Brigand, K., R. Russell, C. Moreilhon, J. M. Rouillard, B. Jost, F. Amiot, V. Magnone, C. Bole-Feysot, P. Rostagno, V. Virolle, et al. 2006. An open-access long oligonucleotide microarray resource for analysis of the human and mouse transcriptomes. Nucleic Acids Res. 34: e87.
18. Smyth, G.K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: article 3.
19. Cesarman, E., R. Dalla-Favera, D. Bentley, and M. Groudine. 1987. Mutations in the first exon are associated with altered transcription of c-myc in Burkitt lymphoma. Science 238: 1272-1275.
20. Lindström, M. S., and K. G. Wiman. 2002. Role of genetic and epigenetic changes in Burkitt lymphoma. Semin. Cancer Biol. 12: 381-387.
21. Pelicci, P. G., D. M. Knowles, II, I. Magrath, and R. Dalla-Favera. 1986. Chromosomal breakpoints and structural alterations of the c-myc locus differ in endemic and sporadic forms of Burkitt lymphoma. Proc. Natl. Acad. Sci. USA 83: 2984-2988. (Pubitemid 16041786)
22. Di Noia, J. M., and M. S. Neuberger. 2007. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76: 1-22.
23. Peled, J. U., F. L. Kuang, M. D. Iglesias-Ussel, S. Roa, S. L. Kalis, M. F. Goodman, and M. D. Scharff. 2008. The biochemistry of somatic hypermutation. Annu. Rev. Immunol. 26: 481-511. (Pubitemid 351600383)
24. Neuberger, M. S., and C. Rada. 2007. Somatic hypermutation: activation-induced deaminase for C/G followed by polymerase η for A/T. J. Exp. Med. 204: 7-10. (Pubitemid 46148749)
25. Kim, J. K., and J. A. Diehl. 2009. Nuclear cyclin D1: an oncogenic driver in human cancer. J. Cell. Physiol. 220: 292-296.
26. Takaki, T., K. Fukasawa, I. Suzuki-Takahashi, K. Semba, M. Kitagawa, Y. Taya, and H. Hirai. 2005. Preferences for phosphorylation sites in the retinoblastoma protein of D-type cyclin-dependent kinases, Cdk4 and Cdk6, in vitro. J. Biochem. 137: 381-386. (Pubitemid 40628445)
27. Wagner, E. F., M. Hleb, N. Hanna, and S. Sharma. 1998. A pivotal role of cyclin D3 and cyclin-dependent kinase inhibitor p27 in the regulation of IL-2-, IL-4-, or IL-10-mediated human B cell proliferation. J. Immunol. 161: 1123-1131. (Pubitemid 28380536)
28. kip1 cyclin-dependent kinase inhibitors is regulated differently during human B cell differentiation. J. Immunol. 165: 4346-4352.
29. Chen, Q., J. Lin, S. Jinno, and H. Okayama. 2003. Overexpression of Cdk6-cyclin D3 highly sensitizes cells to physical and chemical transformation. Oncogene 22: 992-1001. (Pubitemid 36313143)
30. Corcoran, M. M., S. J. Mould, J. A. Orchard, R. E. Ibbotson, R. M. Chapman, A. P. Boright, C. Platt, L. C. Tsui, S. W. Scherer, and D. G. Oscier. 1999. Dysregulation of cyclin dependent kinase 6 expression in splenic marginal zone lymphoma through chromosome 7q translocations. Oncogene 18: 6271-6277.
31. Santamaría, D., C. Barrière, A. Cerqueira, S. Hunt, C. Tardy, K. Newton, J. F. Cáceres, P. Dubus, M. Malumbres, and M. Barbacid. 2007. Cdk1 is sufficient to drive the mammalian cell cycle. Nature 448: 811-815. (Pubitemid 47266342)
32. Pelengaris, S., M. Khan, and G. Evan. 2002. c-MYC: more than just a matter of life and death. Nat. Rev. Cancer 2: 764-776. (Pubitemid 37328911)
33. Smith, S. M., J. Anastasi, K. S. Cohen, and L. A. Godley. 2010. The impact of MYC expression in lymphoma biology: beyond Burkitt lymphoma. Blood Cells Mol. Dis. 45: 317-323.
34. Park, S. S., J. S. Kim, L. Tessarollo, J. D. Owens, L. Peng, S. S. Han, S. Tae Chung, T. A. Torrey, W. C. Cheung, R. D. Polakiewicz, et al. 2005. Insertion of c-Myc into Igh induces B-cell and plasma-cell neoplasms in mice. Cancer Res. 65: 1306-1315. (Pubitemid 40270157)
35. Park, S. S., A. L. Shaffer, J. S. Kim, W. duBois, M. Potter, L. M. Staudt, and S. Janz. 2005. Insertion of Myc into Igh accelerates peritoneal plasmacytomas in mice. Cancer Res. 65: 7644-7652. (Pubitemid 41297237)
36. Wang, J., and L. M. Boxer. 2005. Regulatory elements in the immunoglobulin heavy chain gene 3′-enhancers induce c-myc deregulation and lymphomagenesis in murine B cells. J. Biol. Chem. 280: 12766-12773.
37. Post, S. M., A. Quintás-Cardama, T. Terzian, C. Smith, C. M. Eischen, and G. Lozano. 2010. p53-dependent senescence delays Emu-myc-induced B-cell lymphomagenesis. Oncogene 29: 1260-1269.
38. Guglielmi, L., V. Truffinet, C. Carrion, M. Le Bert, N. Cogné, M. Cogné, and Y. Denizot. 2005. The 5′HS4 insulator element is an efficient tool to analyse the transient expression of an Em-GFP vector in a transgenic mouse model. Transgenic Res. 14: 361-364. (Pubitemid 41125386)
39. Guglielmi, L., M. Le Bert, V. Truffinet, M. Cogné, and Y. Denizot. 2003. Insulators to improve expression of a 3(′)IgH LCR-driven reporter gene in transgenic mouse models. Biochem. Biophys. Res. Commun. 307: 466-471. (Pubitemid 36944954)